Daniel W. Tripp

Estimating Abundance Using Mark–Resight When Sampling Is with Replacement or the Number of Marked Individuals Is Unknown

Although mark-resight methods can often be a less expensive and less invasive means for estimating abundance in long-term population monitoring programs, two major limitations of the estimators are that they typically require sampling without replacement and/or the number of marked individuals available for resighting to be known exactly. These requirements can often be difficult to achieve. Here we address these limitations by introducing the Poisson log and zero-truncated Poisson log-normal mixed effects models (PNE and ZPNE, respectively). The generalized framework of the models allow the efficient use of covariates in modeling resighting rate and individual heterogeneity parameters, information-theoretic model selection and multimodel inference, and the incorporation of individually unidentified marks. Both models may be implemented using standard statistical computing software, but they have also been added to the mark-recapture freeware package Program MARK. We demonstrate the use and advantages of (Z)PNE using black-tailed prairie dog data recently collected in Colorado. We also investigate the expected relative performance of the models in simulation experiments. Compared to other available estimators, we generally found (Z)PNE to be more precise with little or no loss in confidence interval coverage. With the recent introduction of the logit-normal mixed effects model and (Z)PNE, a more flexible and efficient framework for mark-resight abundance estimation is now available for the sampling conditions most commonly encountered in these studies.

Phylogeography of a parasitoid wasp (Diaeretiella rapae): no evidence of host‐associated lineages

The exceptional diversity of insects is often attributed to the effects of specialized relationships between insects and their hosts. Parasite–host interactions are influenced by current natural selection and dispersal, in addition to historical effects that may include past selection, vicariance, and random genetic drift. Both current and historical events can lead to reduced fitness on some hosts. If trade‐offs in fitness on alternate hosts are common, adaptation to one host can prevent adaptation to another, giving rise to genetic differentiation among host‐associated lineages. Previous studies of Diaeretiella rapae (Hymenoptera: Aphidiidae), a parasitoid of aphids, have revealed additive genetic differences in performance between populations that parasitize different aphid host species. To determine whether D. rapae populations collected from different aphid hosts have diverged into genetically independent lineages, we constructed a haplotype network based on sequence variation in mitochondrial DNA (mtDNA). We used single strand conformation polymorphism (SSCP) analysis to examine 2041 base pairs of mtDNA and to identify nucleotide sequences of 42 unique SSCP haplotypes. We found no association between mtDNA haplotypes and host species in either the ancestral range (Europe, Mediterranean region, Middle East, Asia) or part of the introduced range (western North America). Haplotypes likely to be ancestral were geographically widespread and found on both hosts, suggesting that the ability to use both hosts evolved prior to the diversification of the mtDNA. Ongoing gene flow appears to prevent the formation of host races.

Flea Abundance on Black-Tailed Prairie Dogs (Cynomys ludovicianus) Increases During Plague Epizootics

Black-tailed prairie dogs (Cynomys ludovicianus) on the Great Plains of the United States are highly susceptible to plague, caused by the bacterium Yersinia pestis, with mortality on towns during plague epizootics often approaching 100%. The ability of flea-borne transmission to sustain disease spread has been questioned because of inefficiency of flea vectors. However, even with low individual efficiency, overall transmission can be increased if flea abundance (the number of fleas on hosts) increases. Changes in flea abundance on hosts during plague outbreaks were recorded during a large-scale study of plague outbreaks in prairie dogs in north central Colorado during 3 years (2004-2007). Fleas were collected from live-trapped black-tailed prairie dogs before and during plague epizootics and tested by PCR for the presence of Y. pestis. The predominant fleas were two prairie dog specialists (Oropsylla hirsuta and Oropsylla tuberculata cynomuris), and a generalist flea species (Pulex simulans) was also recorded from numerous mammals in the area. The three species differ in seasonal abundance, with greatest abundance in spring (February and March) and fall (September and October). Flea abundance and infestation intensity increased during epizootics and were highest on prairie dogs with Y. pestis-infected fleas. Seasonal occurrence of epizootics among black-tailed prairie dogs was found to coincide with seasonal peaks in flea abundance. Concentration of infected fleas on surviving animals may account for rapid spread of plague during epizootics. In particular, the role of the generalist flea P. simulans was previously underappreciated.

Evidence for the involvement of an alternate rodent host in the dynamics of introduced plague in prairie dogs

1. The introduction of plague to North America is a significant threat to colonies of prairie dogs (Cynomys ludovicianus), a species of conservation concern in the Great Plains. Other small rodents are exposed to the causative agent, Yersinia pestis, during or after epizootics; yet, its effect on these rodents is not known, and their role in transmitting and maintaining plague in the absence of prairie dogs remains unclear. 2. We live-trapped small rodents and collected their fleas on 11 colonies before, during and after plague epizootics in Colorado, USA, from 2004 to 2006. Molecular genetic (polymerase chain reaction) assays were used to identify Y. pestis in fleas. 3. Abundance of northern grasshopper mice (Onychomys leucogaster) was low on sites following epizootics in 2004, and declined markedly following plague onset on other colonies in 2005. These changes coincided with exposure of grasshopper mice to plague, and with periods when mice became infested with large numbers of prairie dog fleas (Oropsylla hirsuta), including some that were infected with Y. pestis. Additionally, several Pleochaetis exilis, fleas restricted to grasshopper mice and never found on prairie dogs on our site, were polymerase chain reaction-positive for Y. pestis, indicating that grasshopper mice can infect their own fleas. No changes in abundance of other rodent species could be attributed to plague, and no other rodents hosted O. hirsuta during epizootics, or harboured Y. pestis-infected fleas. 4. In spring 2004, grasshopper mice were most numerous in colonies that suffered plague the following year, and the pattern of colony extinctions over a 12-year period mirrored patterns of grasshopper mouse abundance in our study area, suggesting that colonies with high densities of grasshopper mice may be more susceptible to outbreaks. We speculate that grasshopper mice help spread Y. pestis during epizootics through their ability to survive infection, harbour prairie dog fleas and, during their wide-ranging movements, transport infected fleas among burrows, which functionally connects prairie dog coteries that would otherwise be socially distinct.

THE POTENTIAL ROLE OF SWIFT FOXES (VULPES VELOX) AND THEIR FLEAS IN PLAGUE OUTBREAKS IN PRAIRIE DOGS

Swift foxes (Vulpes velox) have been proposed as potential carriers of fleas infected with the bacterium Yersinia pestis between areas of epizootics in black-tailed prairie dogs (Cynomys ludovicianus). We examined antibody prevalence rates of a population of swift foxes in Colorado, USA, and used polymerase chain reaction (PCR) assays to examine their flea biota for evidence of Y. pestis. Fifteen of 61 (24%) captured foxes were seropositive, and antibody prevalence was spatially correlated with epizootic plague activity in prairie dog colonies in the year of, and previous to, the study. Foxes commonly harbored the flea Pulex simulans, though none of the fleas was positive for Y. pestis.

Exposure of Small Rodents to Plague during Epizootics in Black-tailed Prairie Dogs

Plague, caused by the bacterium Yersinia pestis, causes die-offs of colonies of prairie dogs (Cynomys ludovicianus). It has been argued that other small rodents are reservoirs for plague, spreading disease during epizootics and maintaining the pathogen in the absence of prairie dogs; yet there is little empirical support for distinct enzootic and epizootic cycles. Between 2004 and 2006, we collected blood from small rodents captured in colonies in northern Colorado before, during, and for up to 2 yr after prairie dog epizootics. We screened 1,603 blood samples for antibodies to Y. pestis, using passive hemagglutination and inhibition tests, and for a subset of samples we cultured blood for the bacterium itself. Of the four species of rodents that were common in colonies, the northern grasshopper mouse (Onychomys leucogaster) was the only species with consistent evidence of plague infection during epizootics, with 11.1–23.1% of mice seropositive for antibody to Y. pestis during these events. Seropositive grasshopper mice, thirteen-lined ground squirrels (Spermophilus tridecemlineatus), and deer mice (Peromyscus maniculatus) were captured the year following epizootics. The appearance of antibodies to Y. pestis in grasshopper mice coincided with periods of high prairie dog mortality; subsequently, antibody prevalence rates declined, with no seropositive individuals captured 2 yr after epizootics. We did not detect plague in any rodents off of colonies, or on colonies prior to epizootics, and found no evidence of persistent Y. pestis infection in blood cultures. Our results suggest that grasshopper mice could be involved in epizootic spread of Y. pestis, and possibly, serve as a short-term reservoir for plague, but provide no evidence that the grasshopper mouse or any small rodent acts as a long-term, enzootic host for Y. pestis in prairie dog colonies.

APPARENT FIELD SAFETY OF A RACCOON POXVIRUS-VECTORED PLAGUE VACCINE IN FREE-RANGING PRAIRIE DOGS (CYNOMYS SPP.), COLORADO, USA

Abstract Prairie dogs (Cynomys spp.) suffer high rates of mortality from plague. An oral sylvatic plague vaccine using the raccoon poxvirus vector (designated RCN-F1/V307) has been developed for prairie dogs. This vaccine is incorporated into palatable bait along with rhodamine B as a biomarker. We conducted trials in August and September 2012 to demonstrate uptake and apparent safety of the RCN-F1/V307 vaccine in two prairie dog species under field conditions. Free-ranging prairie dogs and other associated small rodents readily consumed vaccine-laden baits during field trials with no apparent adverse effects; most sampled prairie dogs (90%) and associated small rodents (78%) had consumed baits. Visual counts of prairie dogs and their burrows revealed no evidence of prairie dog decline after vaccine exposure. No vaccine-related morbidity, mortality, or gross or microscopic lesions were observed. Poxviruses were not isolated from any animal sampled prior to bait distribution or on sites that received placebo baits. We isolated RCN-F1/V307 from 17 prairie dogs and two deer mice (Peromyscus maniculatus) captured on sites where vaccine-laden baits were distributed. Based on these findings, studies examining the utility and effectiveness of oral vaccination to prevent plague-induced mortality in prairie dogs and associated species are underway.

SEASON OF DELTAMETHRIN APPLICATION AFFECTS FLEA AND PLAGUE CONTROL IN WHITE-TAILED PRAIRIE DOG (CYNOMYS LEUCURUS) COLONIES, COLORADO, USA

Abstract In 2008 and 2009, we evaluated the duration of prophylactic deltamethrin treatments in white-tailed prairie dog (Cynomys leucurus) colonies and compared effects of autumn or spring dust application in suppressing flea numbers and plague. Plague occurred before and during our experiment. Overall, flea abundance tended to increase from May or June to September, but it was affected by deltamethrin treatment and plague dynamics. Success in trapping prairie dogs (animals caught/trap days) declined between June and September at all study sites. However, by September trap success on dusted sites (19%; 95% confidence interval [CI] 16–22%) was about 15-fold greater than on undusted control sites (1%; CI 0.3–4%; P≤0.0001). Applying deltamethrin dust as early as 12 mo prior seemed to afford some protection to prairie dogs. Our data showed that dusting even a portion of a prairie dog colony can prolong its persistence despite epizootic plague. Autumn dusting may offer advantages over spring in suppressing overwinter or early-spring flea activity, but timing should be adjusted to precede the annual decline in aboveground activity for hibernating prairie dog species. Large colony complexes or collections of occupied but fragmented habitat may benefit from dusting some sites in spring and others in autumn to maximize flea suppression in a portion of the complex or habitat year-round.

Duration of Plague (Yersinia pestis) Outbreaks in Black-Tailed Prairie Dog (Cynomys ludovicianus) Colonies of Northern Colorado

Plague, caused by the bacterium Yersinia pestis, triggers die-offs in colonies of black-tailed prairie dogs (Cynomys ludovicianus), but the time-frame of plague activity is not well understood. We document plague activity in fleas from prairie dogs and their burrows on three prairie dog colonies that suffered die-offs. We demonstrate that Y. pestis transmission occurs over periods from several months to over a year in prairie dog populations before observed die-offs.

Ecological Traits Driving the Outbreaks and Emergence of Zoonotic Pathogens

Abstract Infectious diseases that are transmitted from wildlife hosts to humans, such as the Ebola virus and MERS virus, can be difficult to understand because the pathogens emerge from complex multifaceted ecological interactions. We use a wildlife–pathogen system—prairie dogs (Cynomys ludovicianus) and the plague bacterium (Yersinia pestis)—to describe aspects of disease ecology that apply to many cases of emerging infectious disease. We show that the monitoring and surveillance of hosts and vectors during the buildup to disease outbreaks are crucial for understanding pathogen-transmission dynamics and that a community-ecology framework is important to identify reservoir hosts. Incorporating multidisciplinary approaches and frameworks may improve wildlife–pathogen surveillance and our understanding of seemingly sporadic and rare pathogen outbreaks.